Broad-ranging low genetic diversity among populations of the yellow finger marsh crab Sesarma rectum Randall, 1840 (Sesarmidae) revealed by DNA barcode

in Crustaceana
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Population genetic studies on marine taxa, specifically in the field of phylogeography, have revealed distinct levels of genetic differentiation in widely distributed species, even though they present long planktonic larval development. A set of factors have been identified as acting on gene flow between marine populations, including physical or physiological barriers, isolation by distance, larval behaviour, and geological and demographic events. In this way, the aim of this study was to analyse the genetic variability among populations of the crab species Sesarma rectum Randall, 1840 along the western Atlantic in order to check the levels of genetic diversity and differentiation among populations. To achieve this purpose, mtDNA cytochrome-c oxidase subunit I (COI) (DNA-barcode marker) data were used to compute a haplotype network and a Bayesian analysis for genetic differentiation, to calculate an Analysis of Molecular Variance (AMOVA), and haplotype and nucleotide diversities. Neutrality tests (Tajima’s D and Fu’s Fs) were accessed, as well as pairwise mismatch distribution under the sudden expansion model. We found sharing of haplotypes among populations of S. rectum along its range of distribution and no significant indication for restricted gene flow between populations separately over 6000 km, supporting the hypothesis of a high dispersive capacity, and/or the absence of strong selective gradients along the distribution. Nevertheless, some results indicated population structure suggesting the presence of two genetic sources (i.e., groups or lineages), probably interpreted as a result of a very recent bottleneck effect due to habitat losses, followed by the beginning of a population expansion.

Broad-ranging low genetic diversity among populations of the yellow finger marsh crab Sesarma rectum Randall, 1840 (Sesarmidae) revealed by DNA barcode

in Crustaceana



AbeleL. G.1992. A review of the grapsid crab genus Sesarma (Crustacea: Decapoda: Grapsidae) in America, with the description of a new genus. Smithsonian Contribution to Zoology527: 1-60.

AddisonJ. A.OrtB. S.MesaK. A.PogsonG. H.2008. Range-wide genetic homogeneity in the California sea mussel (Mytilus californianus): a comparison of allozymes, nuclear DNA markers, and mitochondrial DNA sequences. Molecular Ecology17: 4222-4232.

AltukhovY. P.1981. The stock concept from the viewpoint of population genetics. Canadian Journal of Fisheries and Aquatic Sciences38: 1523-1538.

AngerK.MoreiraG. S.2004. Biomass and elemental composition of eggs and larvae of a magrove crab, Sesarma rectum Randall (Decapoda: Sesarmidae) and comparison to a related species with abbreviated larval development. Scientia Marina68: 117-126.

Aris-BrosouS.ExcoffierL.1996. The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Molecular Biology and Evolution13: 494-504.

AviseJ. C.2004. Molecular markers natural history and evolution (2nd ed.): 1-532. (Sinauer & AssociatesSunderland, MA).

AviseJ. C.2009. Phylogeography: retrospect and prospect. Journal of Biogeography36: 3-15.

BarberP. H.PalumbiS. R.ErdmannM. V.MoosaM. K.2000. A marine Wallace’s line? Nature406: 692-693.

BurtonR. S.1983. Protein polymorphisms and genetic differentiation of marine invertebrate populations. Marine Biology Letters4: 193-206.

BurtonR. S.FeldmanM. W.1982. Population genetics of coastal and estuarine invertebrates: does larval behavior influence population structure? In: KennedyV. S. (ed.) Estuarine comparisons: 537-551. (Academic PressSan Diego, CA).

Carvalho-BatistaA.NegriM.PileggiL. G.CastilhoA. L.CostaR. C.MantelattoF. L.2014. Inferring population connectivity across the range of distribution of the stiletto shrimp Artemesia longinaris Spence Bate, 1888 (Decapoda, Penaeidae) from DNA barcoding: implications for fishery management. ZooKeys457: 271-288.

ChustG.VillarinoE.ChenuilA.IrigoienX.BizselN.BodeA.BromsC.ClausS.PuellesM. L. F.Fonda-UmaniS.HoarauG.MazzocchiM. G.MozetičP.VandepitteL.VeríssimoH.ZervoudakiS.BorjaA.2016. Dispersal similarly shapes both population genetics and community patterns in the marine realm. Scientific Reports6: 28730.

CiranoM.MataM. M.CamposE. J. D.DeirN. F. R.2006. A circulação oceânica de larga-escala na região oeste do Atlântico Sul com base no modelo de circulação global OCCAM. Revista Brasileira de Geofísica24: 209-230.

ClementM.PosadaD.CrandallK. A.2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology9: 1657-1660.

CoranderJ.GyllenbergM.KoskiT.2007. Random partition models and exchangeability for Bayesian identification of population structure. Bulletin of Mathematical Biology69: 797-815.

CoranderJ.WaldmannP.MarttinenP.SillanpääM. J.2004. BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics20: 2363-2369.

CoranderJ.WaldmannP.SillanpääM. J.2003. Bayesian analysis of genetic differentiation between populations. Genetics163: 367-374.

CowenR. K.KamazimaM. M. L.SponaugleS.ParisC. B.OlsonD. B.2000. Connectivity or marine populations: open or closed? Science287: 857-859.

ExcoffierL.LanganeyA.1989. Origin and differentiation of human mitochondrial DNA. American Journal of Human Genetics44: 73-85.

ExcoffierL.LavalG.SchneiderS.2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online1: 47-50.

ExcoffierL.SmouseP. E.QuattroJ. M.1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics131: 479-491.

FelderD. L.StatonJ. L.1994. Genetic differentiation in trans-Floridian species complexes of Sesarma and Uca (Decapoda: Brachyura). Journal of Crustacean Biology14: 191-209.

FerreiraA. L.LacerdaL. D.2016. Degradation and conservation of Brazilian mangroves, status and perspectives. Ocean & Coastal Management125: 38-46.

FuY. X.1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics146: 915-925.

GopurenkoD.HughesJ. M.2002. Regional patterns of genetic structure among Australian populations of the mud crab, Scylla serrata (Crustacea: Decapoda): evidence from mitochondrial DNA. Marine and Freshwater Research53: 849-857.

GrantW. S.BowenB. W.1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. Journal of Heredity89: 415-426.

HallT. A.1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series41: 95-98.

HamasakiK.IizukaC.OjimaA.SugizakiM.SugimotoM.ShigekiD.KitadaS.2015. Genetic diversity and demographic history of the terrestrial hermit crabs Birgus latro and Coenobita brevimanus in the north-western Pacific region. Journal of Crustacean Biology35(6): 793-803.

HarpendingH.1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology66: 591-600.

HedgecockD.1986. Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bulletin of Marine Science39: 550-564.

HellbergM. E.BurtonR. S.NeigelJ. E.PalumbiS. R.2002. Genetic assessment of connectivity among marine populations. Bulletin of Marine Science70: 273-290.

ItuarteR. B.D’AnatroA.LuppiT. A.RibeiroP. D.SpivakE. D.IribarneO. O.LessaE. P.2012. Population structure of the SW Atlantic estuarine crab Neohelice granulata throughout its range: a genetic and morphometric study. Estuarine and Coasts35: 1249-1260.

KellyR. P.PalumbiS. R.2010. Genetic structure among 50 species of the northeastern Pacific rocky intertidal community. PLoS ONE5: e8594.

KimuraM.WeissG. H.1964. The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics49: 561-576.

KoehnR. K.1969. Esterase heterogeneity: dynamics of a polymorphism. Science163: 943-944.

LacerdaL. D.MenezesM. O. T.MolisaniM. M.2007. Changes in mangrove extension at the Pacoti River estuary, CE, NE Brazil due to regional environmental changes between 1958 and 2004. Biota Neotropica7: 67-72.

LaurenzanoC.CostaT. M.SchubartC. D.2016. Contrasting patterns of clinal genetic diversity and potential colonization pathways in two species of western Atlantic fiddler crabs. PLoS ONE11: e0166518.

LaurenzanoC.FaríasN. E.SchubartC. D.2012. Mitochondrial genetic structure of two populations of Uca uruguayensis fails to reveal an impact of the Rio de la Plata on gene flow. Nauplius20: 15-25.

LaurenzanoC.MantelattoF. L.SchubartC. D.2013. South American homogeneity versus Caribbean heterogeneity: population genetic structure of the western Atlantic fiddler crab Uca rapax (Brachyura, Ocypodidae). Journal of Experimental Marine Biology and Ecology449: 22-27.

LeeS. Y.1998. Ecological role of grapsid crabs in mangrove ecosystems: a review. Marine and Freshwater Research49: 335-343.

MantelattoF. L.RoblesR.BiagiR.FelderD. L.2006. Molecular analysis of the taxonomic and distributional status for the hermit crab genera Loxopagurus Forest, 1964 and Isocheles Stimpson, 1858 (Decapoda, Anomura, Diogenidae). Zoosystema28: 495-506.

McMillen-JacksonA. L.BertT. M.2004. Mitochondrial DNA variation and population genetic structure of the blue crab Callinectes sapidus in the eastern United States. Marine Biology145: 769-777.

McMillen-JacksonA. L.BertT. M.SteeleP.1994. Population genetics of the blue crab Callinectes sapidus: modest population structuring in a background of high gene flow. Marine Biology118: 53-65.

MeloG. A. S.1996. Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro: 1-604. (PlêiadeSão Paulo).

MillerS. A.DykesD. D.PoleskyH. F.1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research16(3): 1215.

NeiM.MarayumaT.ChakrabortyR.1975. The bottleneck effect and genetic variability in populations. Evolution29: 1-10.

Oliveira-NetoJ. F.PieM. R.ChammasM. A.OstrenskyA.BoegerW. A.2008. Phylogeography of the blue land crab, Cardisoma guanhumi (Decapoda: Gecarcinidae) along the Brazilian coast. Journal of the Marine Biological Association of the United Kingdom88: 1417-1423.

PalumbiS. R.1994. Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology and Systematics25: 547-572.

PalumbiS. R.2003. Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications13: s146-s158.

PatarnelloT.VolckaertF. A. M.CastilhoR.2007. Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Molecular Ecology16: 4426-4444.

Rodríguez-ReyG. T.Solé-CavaA. M.LazoskiC.2014. Genetic homogeneity and historical expansions of the slipper lobster, Scyllarides brasiliensis, in the south-west Atlantic. Marine and Freshwater Research65: 59-69.

RogersA. R.1995. Genetic evidence for a Pleistocene population explosion. Evolution49: 608-615.

RogersA. R.HarpendingH.1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution9: 552-569.

RozasJ.RozasR.1999. DnaSP version 3.0: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics15: 174-175.

RymanN.UtterF.LaikreL.1995. Protection of intraspecific biodiversity of exploited fishes. Reviews in Fish Biology and Fisheries5: 417-446.

SambrookJ.FritschE. F.ManiatisT.1989. In vitro amplification of DNA by the polymerase chain reaction. In: SambrookJ.FritschE. F.ManiatisT. (eds.) Molecular cloning: a laboratory manual: 14.1-14.35. (Cold Spring Harbor Laboratory PressNew York, NY).

ScheltemaR. S.1986. On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview. Bulletin of Marine Science39: 290-322.

SchneiderS.ExcoffierL.1999. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics152: 1079-1089.

SchubartC. D.HorstD.DieselR.1999. First record of Sesarma rectum Randall (Brachyura, Grapsidae, Sesarminae) from the Lesser Antilles. Crustaceana72: 537-538.

SchubartC. D.HuberM. G. J.2006. Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bulletin Français de la Pêche et de la Pisciculture380-381: 1019-1028.

ShanksA. L.2009. Pelagic larval duration and dispersal distance revisited. Biological Bulletin216: 373-385.

ShanksA. L.GranthamB. A.CarrM. H.2003. Propagule dispersal distance and the size and spacing of marine reserves. Ecological Applications13: S159-S169.

SilvaI. C.MesquitaN.PaulaJ.2010. Lack of population structure in the fiddler crab Uca annulipes along an East African latitudinal gradient: genetic and morphometric evidence. Marine Biology157: 1113-1126.

SpencerC. C.NeigelJ. E.LebergP. L.2000. Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Molecular Ecology9: 1517-1528.

TajimaF.1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics123: 585-595.

TavaresM. S.AlbuquerqueE. F.1989. Levantamento preliminar dos Brachyura (Crustacea: Decapoda) da lagoa de Itaipu, Rio de Janeiro, Brasil. Atlântica11: 101-108.

TaylorM. S.HellbergM. E.2003. Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science299: 107-109.

TeodoroS. S. A.TerossiM.CostaR. C.MantelattoF. L.2015. Genetic homogeneity in the commercial pink shrimp Farfantepenaeus paulensis revealed by COI barcoding gene. Estuarine Coastal and Shelf Science166: 1-7.

TerossiM.MantelattoF. L.2012. Morphological and genetic variability in Hippolyte obliquimanus Dana, 1852 (Decapoda, Caridea, Hippolytidae) from Brazil and the Caribbean Sea. Crustaceana85: 685-712.

ThompsonJ. D.HiggingD. G.GibsonT. J.1994. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting specific gap penalties and weight matrix choice. Nucleic Acids Research22: 4673-4680.

WaplesR. S.1987. A multispecies approach to the analysis of gene flow in marine shore fishes. Evolution41: 385-400.

WarnerR. R.CowenR. K.2002. Local retention of production in marine populations: evidence, mechanisms, and consequences. Bulletin of Marine Science70(1): 245-249.

WiemanA. C.BerendzenP. B.HamptonK. R.JangJ.HopkinsM. J.JurgensonJ.McNamaraJ. C.ThurmanC. L.2014. A panmictic fiddler crab from the coast of Brazil? Impact of divergent ocean currents and larval dispersal potential on genetic and morphological variation in Uca maracoani. Marine Biology161: 173-185.

WilliamsS. T.BenzieJ. A. H.1993. Genetic consequences of long larval life in the starfish Linckia laevigata (Echinodermata: Asteroidea) on the Great Barrier Reef. Marine Biology117: 71-77.

WrightS.1931. Evolution in Mendelian populations. Genetics16: 97-159.

WrightS.1943. Isolation by distance. Genetics38: 114-138.

WrightS.1978. Evolution and the genetics of populations 4 Variability within and among natural populations: 1-590. (University of Chicago PressChicago, IL).


  • View in gallery

    Sample sites of Sesarma rectum Randall, 1840 along the western Atlantic. Coloured dots indicate the locations of the populations used in the analyses. Shaded areas indicate the reported distribution of S. rectum (countries indicated). PA, Pará; CE, Ceará; RN, Rio Grande do Norte; AL, Alagoas; BA, Bahia; ES, Espírito Santo; SP, São Paulo.

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    Parsimony haplotype network for mtDNA COI from the populations of Sesarma rectum Randall, 1840, with the distribution of the 13 haplotypes (H) identified. The size of the circles is proportional to the haplotype frequency. Numbers inside haplotypes indicate the number of individuals within the haplotype if present more than once. Black circles indicate the median vector. Different colours represent different populations. PA, Pará; CE, Ceará; RN, Rio Grande do Norte; AL, Alagoas; BA, Bahia; ES, Espírito Santo; SP, São Paulo.

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    Graphic generated by Bayesian analysis for genetic differentiation for mtDNA COI among populations of Sesarma rectum Randall, 1840, indicating the grouping of two clusters supported by a posterior probability value of 1. Haplotypes (H) belonging to each cluster are indicated. Different colours represent different populations. See fig. 2 for haplotypes relationships and colour of populations.

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    Mismatch distribution for mtDNA COI of Sesarma rectum Randall, 1840 under the models of demographic (A) and spatial (B) expansion, showing the frequency distribution of the number of pairwise nucleotide differences among all individuals.


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